Study of the removal of Polycyclic Aromatic Hydrocarbons by a halotolerant bacteria isolated from Dehloran Oil-contaminated soil
Subject Areas :
Environmental Microbiology
Maryam Firoozbakht
1
,
Abbas Akhavan Sepahi
2
,
Hamid Rashedi
3
,
Fatemeh Yazdian
4
1 - PhD student, Department of Biology, Faculty of convergent sciences and technologies, Science and Research Branch, Islamic Azad University, Tehran, Iran.
2 - Department of Microbiology, School of Biological Sciences, Islamic Azad University, North Tehran Branch, Tehran, Iran
3 - Associate Professor, Department of Chemical Engineering, Tehran University, Tehran, Iran.
4 - Associate Professor, Faculty of New Science and Technologies, University of Tehran, Tehran, Iran
Received: 2022-12-23
Accepted : 2023-05-31
Published : 2023-06-05
Keywords:
Biosurfactant,
Polycyclic Aromatic Hydrocarbons,
Environment contaminant removal,
Key words: Halotolerant bacteria,
Labedella gwakjiensis strain KDI,
Abstract :
Background and Objectives: Soil contamination by petroleum compounds and salt often occurs simultaneously. The aim of this study was the isolation of halotolerant bacterial strains with the ability to remove different concentrations of polycyclic aromatic hydrocarbons (PAHs).
Material and Methods: In the present original study, petroleum-contaminated soil samples were collected from Dehlran area. To isolate bacterial strains degrading PAHs, PAHs- enriched media were used as the sole source of carbon and energy. The ability of the isolates to tolerate different salt concentrations was investigated. Based on its capacity to produce biosurfactants, a suitable bacterial strain was chosen and the biodegradation of various types of PAHs was evaluated. The effects of the molecular weight and initial concentration of different types of PAHs on the strain’s cell growth and biodegradation were investigated.
Results: Among the isolates, Labedella gwakjiensis strain KDI, with the ability to grow at concentrations greater than 3% salt and produce biosurfactants, was selected. The results demonstrated that this strain could biodegrade various types of PAHs, and that the molecular weight and initial concentration of PAHs, which have a direct effect on cell growth, indirectly affect the biodegradation rate.
Conclusion: Salt is considered as a deterrent in biodegradation. Hence the use of halotolerant bacterial strains capable of biodegrading PAHs is critical in removing these pollutants from the environment.
References:
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Lee BB, Chan ES, Ravindra P, Khan TA. Surface tension of viscous biopolymer solutions measured using the du Nouy ring method and the drop weight methods. Polym. Bull. 69: 471-489. 2012. https://doi.org/10.1007/s00289-012-0782-2
Lillo A, Ashley FP, Palmer RM, Munson MA, Kyriacou L, Weightman AJ, Wade WG. Novel subgingival bacterial phylotypes detected using multiple universal polymerase chain reaction primer sets. Oral Microbiol Immunol. 2006; 21:61–68
Feng L, Chen Y, Ren J, Qu X. A graphene functionalized electrochemical aptasensor for selective label-free detection of cancer cells. Biomaterials. 2011; 32:2930–2937
Firoozbakht M, Sepahi AA, Rashedi H, Yazdian F. Investigating the effect of nanoparticle on phenanthrene biodegradation by Labedella gwakjiensis strain KDI. Biodegradation. 2022; 33(5):441-460. https://doi.org/10.1007/s10532-022-09991-0
Caglar G B, Eker S G. Prediction of Polycyclic Aromatic Hydrocarbons (PAHs) Removal from Wastewater Treatment Sludge Using Machine Learning Methods. Water Air Soil Pollut. 2021; 232: 87. https://doi.org/10.1007/s11270-021-05049-8
Al Farraj DA, Elshikh MS, Al Khulaifi MM, Hadibarata T, Yuniarto A, Syafiuddin A. Biotransformation, and detoxification of antraquione dye green 3 using halophilic Hortaea sp. Int Biodeterior Biodegrad. 2019; 140:72–77
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Aghaei S. S, Fakharian, Zolfaghary M. R, Soleimani M. Production and characterization of biosurfactant by indigenous halotolerant Microbacterium sp., isolated from Qom saline soils lake. Journal of Microbial World, 2020; 12(4): 423-438
Sun S, Wang Y, Zang T, Wei J, Wu H, Wei C, Qiu G, Li F. A biosurfactant–producing Pseudomonas aeruginosa S5 isolated from coking wastewater and its application for bioremediation of polycyclic aromatic hydrocarbons. Bioresour. Technol. 2019; 281: 421–428.
Gharaei S, Ohadi M, Hassanshahian M, Porsheikhali S, Forootanfar H. Isolation, Optimization, and Structural Characterization of Glycolipid Biosurfactant Produced by Marine Isolate Shewanella algae B12 and Evaluation of Its Antimicrobial and Anti-biofilm Activity. Appl Biochem Biotechnol. 2022;194(4):1755-1774. doi: 10.1007/s12010-021-03782-8.
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Govarthanan M, Khalifa AY, Kamala-Kannan S, Srinivasan P, Selvankumar T, Selvam K, Kim W. Significance of allochthonous brackish water Halomonas sp. on biodegradation of low and high molecular weight polycyclic aromatic hydrocarbons. Chemosphere. 2020; 243:125389.
Sivaram AK, Logeshwaran P, Lockington R, Naidu R, Megharaj M. Low molecular weight organic acids enhance the high molecular weight polycyclic aromatic hydrocarbons degradation by bacteria. Chemosphere. 2019; 222:132-140.
Sakshi, Singh SK, Haritash AK. Catabolic enzyme activities during biodegradation of three-ring PAHs by novel DTU-1Y and DTU-7P strains isolated from petroleum-contaminated soil. Arch Microbiol. 2021;203(6):3101-3110. https://doi.org/10.1007/s00203-021-02297-4
36. Bacosa H. P, Kang A, Lu K, Liu Z. Initial oil concentration affects hydrocarbon biodegradation rates and bacterial community composition in seawater. Marine pollution bulletin. 2021; 162, 111867. https://doi.org/1016/j.marpolbul.2020.111867
Rabani MS, Sharma R, Singh R, Gupta M.K. Characterization and Identification of Naphthalene Degrading Bacteria Isolated from Petroleum Contaminated Sites and Their Possible Use in Bioremediation, Polycyclic Aromatic Compounds. 2022; 42:3, 978-989, https://doi.org/10.1080/10406638.2020.1759663
Kong X, Dong R, King T, Chen F, Li H. Biodegradation Potential of Bacillus sp. PAH-2 on PAHs for Oil-Contaminated Seawater. Molecules. 2022; 27(3):687. https://doi.org/10.3390/molecules27030687
Zhong Y, Luan T, Wang X, Lan C, Tam N.F. Influence of growth medium on cometabolic degradation of polycyclic aromatic hydrocarbons by Sphingomonas sp. strain PheB4. Appl. Microbiol. Biotechnol. 2007; 75, 175e186. https://doi.org/10. 1007/s00253-006-0789-4.
Xu M, Wu M, Zhang Y, Zhang H, Liu W, Chen G, Xiong G, Guo L. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by bacterial mixture. Int. J. Environ. Sci. Technol. 2022; 19: 3833–3844 https://doi.org/10.1007/s13762-021-03284-4
41. Wang Y, Nie M, Diwu Z, Chang F, Nie H, Zhang B, Bai X, Yin Q. Toxicity evaluation of the metabolites derived from the degradation of phenanthrene by one of a soil ubiquitous PAHs-degrading strain Rhodococcus qingshengii FF. J. Hazard. Mater. 2021; 415: 125657. https://doi.org/10.1016/j.jhazmat.2021.125657
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Dai C, Han Y, Duan Y, Lai X, Fu R, Liu S, Leong KH, Tu Y, Zhou L. Review on the contamination and remediation of polycyclic aromatic hydrocarbons (PAHs) in coastal soil and sediments. Environ Res. 2022; 205:112423. https:/ doi: 10.1016/j.envres.2021.112423
Xingjian Xu, Wenming Liu, Wei Wang, Shuhua Tian, Pan Jiang, Qige Qi, Fengjiao Li, Haiyan Li, Quanying Wang, Huai Li, Hongwen Yu. Potential biodegradation of phenanthrene by isolated halotolerant bacterial strains from petroleum oil polluted soil in Yellow River Delta. Sci. Total Environ. 2019; 664:1030-1038. https://doi.org/10.1016/j.scitotenv.2019.02.080
Mallah M. A, Changxing L, Mallah M. A, Noreen S, Liu Y, Saeed M, Xi H, Ahmed B, Feng F, Mirjat A. A, Wang W, Jabar A, Naveed M, Li J. H, Zhang Q. Polycyclic aromatic hydrocarbon, and its effects on human health: An overeview. Chemosphere. 2022; 296:133948. https://doi.org/10.1016/j.chemosphere.2022.133948
Gupte A, Tripathi A, Patel H, Rudakiya D, Gupte S. Bioremediation of polycyclic aromatic hydrocarbon (PAHs): A perspective. Open Biotechnol J. 2016; 10:363-368.
Imam A, Kumar Suman S, Kanaujia PK, Ray A. Biological machinery for polycyclic aromatic hydrocarbons degradation: A review. Bioresour Technol. 2022; 343:126121. https://doi:10.1016/j.biortech.2021.126121
Kuppusamy S, Thavamani P, Megharaj M, Naidu R. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by novel bacterial consortia tolerant to diverse physical settings - Assessments in liquid- and slurry-phase systems. Int Biodeterior Biodegradation. 2016; 108:149-157. http://dx.doi.org/10.1016/j.ibiod.2015.12.013
Bastiaens L, Springael D, Wattiau P, Harms H, Verachtert H, Diels L. Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl. Environ. Microbiol. 2000; 66:1834-1843
Subashchandrabose S. R, Venkateswarlu K, Naidu R, Megharaj M. Biodegradation of high-molecular weight PAHs by Rhodococcus wratislaviensis strain 9: Overexpression of amidohydrolase induced by pyrene and BaP. Sci Total Environ. 2019; 651(1): 813–821. https://doi.org/10.1016/j.scitotenv.2018.09.192
Akbari A, David C, Rahim A A, Ghoshal S. Salt selected for hydrocarbon-degrading bacteria and enhanced hydrocarbon biodegradation in slurry bioreactors. Water Res. 2021; 202:117424. https://doi.org/10.1016/j.watres.2021.117424
Al Farraj D. A, Hadibarata T, Yuniarto A, Alkufeidy R. M, Alshammari M. K, Syafiuddin A. Exploring the potential of halotolerant bacteria for biodegradation of polycyclic aromatic hydrocarbon. Bioprocess and biosystems engineering. 2020; 43(12):2305–2314. https://doi.org/10.1007/s00449-020-02415-4
Pourbabaee A.A, Shahriari M.H, Garousin H. Biodegradation of phenanthrene as a model hydrocarbon: Power display of a super-hydrophobic halotolerant enriched culture derived from a saline-sodic soil. Biotechnol Rep. 2019; 24: e00388. https://doi.org/10.1016/j.btre.2019.e00388
Ghorbannezhad H, Moghimi H, Dastgheib SMM. Biodegradation of high molecular weight hydrocarbons under saline condition by halotolerant Bacillus subtilis and its mixed cultures with Pseudomonas species. Sci Rep. 2022; 2;12(1):13227. doi: 10.1038/s41598-022-17001-9
Rahimi E. S, Fooladi J, ebrahimipour G, Soudi M. R, Fooladi T. Isolation of fluorene degrading microorganisms from sediments of the Southern Caspian Sea Coasts and evaluation of their bioremediation potential. Journal of Microbial World. 2020; 13(13): 239-252 [In Persian]
Orgiazzi A, Ballabio C, Panagos P, Jones A, Fernández-Ugalde O. LUCAS Soil, the largest expandable soil dataset for Europe: A review. Eur J Soil Sci. 2018; 69: 140–153. https://doi.org/10.1111/ejss.12499
Jorfi S, Mohamadiyan G, Jaafarzadeh N, Esrafili A, Akbari H, Ali G. Bioremediation of Pyrene-Contaminated Soils Using Biosurfactant. Jentashapir Journal of Health Research. 2014; 5(5): e23228. https://doi.org/10.17795/jjhr-23228.
Dastgheib S.M, Amoozegar M.A, Khajeh K, Shavandi M, Ventosa A. Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol. 2012; 95(3):789–798. https://doi.org/10.1007/s00253-011-3706-4
Lin M, Hu X, Chen W, Wang H, Wang C. Biodegradation of phenanthrene by Pseudomonas sp. BZ-3, isolated from crude oil contaminated soil. Int Biodeterior Biodegradation. 2014; 94: 176–181. http://dx.doi.org/10.1016/j.ibiod.2014.07.011
Liu X. X, Hu X, Cao Y, Pang W. J, Huang J. Y, Guo P, Huang L. Biodegradation of Phenanthrene and Heavy Metal Removal by Acid-Tolerant Burkholderia fungorum FM-2. Front Microbiol. 2019; 10: 408. https://doi.org/10.3389/fmicb.2019.00408
Akhavan Sepahi.A, Dejban golpasha, Emami.M, Nakhoda.A.M. Isolation and characterization of crude oil degrading Bacillus spp. Iran.J.Environ.Health.Sci.Eng. 2008; 5:149-154.
Nogueira Felix AK, Martins JJL, Lima Almeida JG, Giro MEA, Cavalcante KF, Maciel Melo VM, Loiola Pessoa OD, Ponte Rocha MV, Rocha Barros Gonçalves L, Saraiva de Santiago Aguiar R. Purification and characterization of a biosurfactant produced by Bacillus subtilis in cashew apple juice and its application in the remediation of oil-contaminated soil. Colloids Surf B. 2019; 175:256-263. https://doi:10.1016/j.colsurfb.2018.11.062
Reddy MS, Naresh B, Leela T, Prashanthi M, Madhusudhan N.Ch, Dhanasri G, Prathibha Devi. Biodegradation of phenanthrene with biosurfactant production by a new strain of Brevibacillus sp. Bioresour Technol. 2010; 101(20):7980-7983. https://doi.org/10.1016/j.biortech.2010.04.054
Lee BB, Chan ES, Ravindra P, Khan TA. Surface tension of viscous biopolymer solutions measured using the du Nouy ring method and the drop weight methods. Polym. Bull. 69: 471-489. 2012. https://doi.org/10.1007/s00289-012-0782-2
Lillo A, Ashley FP, Palmer RM, Munson MA, Kyriacou L, Weightman AJ, Wade WG. Novel subgingival bacterial phylotypes detected using multiple universal polymerase chain reaction primer sets. Oral Microbiol Immunol. 2006; 21:61–68
Feng L, Chen Y, Ren J, Qu X. A graphene functionalized electrochemical aptasensor for selective label-free detection of cancer cells. Biomaterials. 2011; 32:2930–2937
Firoozbakht M, Sepahi AA, Rashedi H, Yazdian F. Investigating the effect of nanoparticle on phenanthrene biodegradation by Labedella gwakjiensis strain KDI. Biodegradation. 2022; 33(5):441-460. https://doi.org/10.1007/s10532-022-09991-0
Caglar G B, Eker S G. Prediction of Polycyclic Aromatic Hydrocarbons (PAHs) Removal from Wastewater Treatment Sludge Using Machine Learning Methods. Water Air Soil Pollut. 2021; 232: 87. https://doi.org/10.1007/s11270-021-05049-8
Al Farraj DA, Elshikh MS, Al Khulaifi MM, Hadibarata T, Yuniarto A, Syafiuddin A. Biotransformation, and detoxification of antraquione dye green 3 using halophilic Hortaea sp. Int Biodeterior Biodegrad. 2019; 140:72–77
Sarubbo L, Silva M, Durval I, Bezerra K, Ribeiro B, Silva I, Twigg M, Banat I, Biosurfactants: Production, properties, applications, trends, and general perspectives, Biochem. Eng. J. 2022; 181 https://doi.org/10.1016/j.bej.2022.108377.37.
Aghaei S. S, Fakharian, Zolfaghary M. R, Soleimani M. Production and characterization of biosurfactant by indigenous halotolerant Microbacterium sp., isolated from Qom saline soils lake. Journal of Microbial World, 2020; 12(4): 423-438
Sun S, Wang Y, Zang T, Wei J, Wu H, Wei C, Qiu G, Li F. A biosurfactant–producing Pseudomonas aeruginosa S5 isolated from coking wastewater and its application for bioremediation of polycyclic aromatic hydrocarbons. Bioresour. Technol. 2019; 281: 421–428.
Gharaei S, Ohadi M, Hassanshahian M, Porsheikhali S, Forootanfar H. Isolation, Optimization, and Structural Characterization of Glycolipid Biosurfactant Produced by Marine Isolate Shewanella algae B12 and Evaluation of Its Antimicrobial and Anti-biofilm Activity. Appl Biochem Biotechnol. 2022;194(4):1755-1774. doi: 10.1007/s12010-021-03782-8.
Zang T, Wu H, Yan B, Zhang Y, Wei C. Enhancement of PAHs biodegradation in biosurfactant/phenol system by increasing the bioavailability of PAHs. Chemosphere. 2021; 266:128941. https:// doi: 10.1016/j.chemosphere.2020.128941
Govarthanan M, Khalifa AY, Kamala-Kannan S, Srinivasan P, Selvankumar T, Selvam K, Kim W. Significance of allochthonous brackish water Halomonas sp. on biodegradation of low and high molecular weight polycyclic aromatic hydrocarbons. Chemosphere. 2020; 243:125389.
Sivaram AK, Logeshwaran P, Lockington R, Naidu R, Megharaj M. Low molecular weight organic acids enhance the high molecular weight polycyclic aromatic hydrocarbons degradation by bacteria. Chemosphere. 2019; 222:132-140.
Sakshi, Singh SK, Haritash AK. Catabolic enzyme activities during biodegradation of three-ring PAHs by novel DTU-1Y and DTU-7P strains isolated from petroleum-contaminated soil. Arch Microbiol. 2021;203(6):3101-3110. https://doi.org/10.1007/s00203-021-02297-4
36. Bacosa H. P, Kang A, Lu K, Liu Z. Initial oil concentration affects hydrocarbon biodegradation rates and bacterial community composition in seawater. Marine pollution bulletin. 2021; 162, 111867. https://doi.org/1016/j.marpolbul.2020.111867
Rabani MS, Sharma R, Singh R, Gupta M.K. Characterization and Identification of Naphthalene Degrading Bacteria Isolated from Petroleum Contaminated Sites and Their Possible Use in Bioremediation, Polycyclic Aromatic Compounds. 2022; 42:3, 978-989, https://doi.org/10.1080/10406638.2020.1759663
Kong X, Dong R, King T, Chen F, Li H. Biodegradation Potential of Bacillus sp. PAH-2 on PAHs for Oil-Contaminated Seawater. Molecules. 2022; 27(3):687. https://doi.org/10.3390/molecules27030687
Zhong Y, Luan T, Wang X, Lan C, Tam N.F. Influence of growth medium on cometabolic degradation of polycyclic aromatic hydrocarbons by Sphingomonas sp. strain PheB4. Appl. Microbiol. Biotechnol. 2007; 75, 175e186. https://doi.org/10. 1007/s00253-006-0789-4.
Xu M, Wu M, Zhang Y, Zhang H, Liu W, Chen G, Xiong G, Guo L. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by bacterial mixture. Int. J. Environ. Sci. Technol. 2022; 19: 3833–3844 https://doi.org/10.1007/s13762-021-03284-4
41. Wang Y, Nie M, Diwu Z, Chang F, Nie H, Zhang B, Bai X, Yin Q. Toxicity evaluation of the metabolites derived from the degradation of phenanthrene by one of a soil ubiquitous PAHs-degrading strain Rhodococcus qingshengii FF. J. Hazard. Mater. 2021; 415: 125657. https://doi.org/10.1016/j.jhazmat.2021.125657
